Activation of TRPA1 on dural afferents: A potential mechanism of headache pain

Pain

Volumn 153, Issue 9, 2012, Pages 1949-1958

  Edelmayer, Rebecca M ^a   Le, Larry N ^a   Yan, Jin ^a   Wei, Xiaomei ^a   Nassini, Romina ^b   Materazzi, Serena ^b   Preti, Delia ^c   Appendino, Giovanni ^d   Geppetti, Pierangelo ^b   Dodick, David W ^e   Vanderah, Todd W ^a   Porreca, Frank ^a   Dussor, Gregory ^a  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF FLORENCE   (Italy)

^c UNIVERSITY OF FERRARA   (Italy)

^d UNIVERSITY OF EASTERN PIEDMONT   (Italy)

^e MAYO CLINIC   (United States)

Author keywords

Allodynia; Dura; Headache; Migraine; Mustard oil; TRPA1; Umbellulone

Indexed keywords

ALLYL ISOTHIOCYANATE; ANTIMIGRAINE AGENT; HC 030031; IRRITANT AGENT; SUMATRIPTAN; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1; UMBELLULONE; UNCLASSIFIED DRUG;

ALLODYNIA; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHANNEL GATING; CONTROLLED STUDY; DURA MATER; ELECTRIC CURRENT; EXPLORATORY BEHAVIOR; FACE PAIN; IN VITRO STUDY; LEG PAIN; MALE; MIGRAINE; NERVE CELL CULTURE; NERVE CONDUCTION; NONHUMAN; OPEN FIELD BEHAVIOR; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SENSORY NERVE; SIGNAL TRANSDUCTION; SKIN PAIN; TACTILE STIMULATION; TRIGEMINUS GANGLION;

ANIMALS; DURA MATER; HEADACHE; IRRITANTS; MALE; MONOTERPENES; MUSTARD PLANT; NEURONS, AFFERENT; PATCH-CLAMP TECHNIQUES; PLANT OILS; RATS; RATS, SPRAGUE-DAWLEY; TRIGEMINAL GANGLION; TRPC CATION CHANNELS;

EID: 84864609778     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1016/j.pain.2012.06.012     Document Type: Article

References (60)

1. E. Andre, B. Campi, S. Materazzi, M. Trevisani, S. Amadesi, D. Massi, C. Creminon, N. Vaksman, R. Nassini, M. Civelli, P.G. Baraldi, D.P. Poole, N.W. Bunnett, P. Geppetti, and R. Patacchini Cigarette smoke-induced neurogenic inflammation is mediated by alpha, beta-unsaturated aldehydes and the TRPA1 receptor in rodents J Clin Invest 118 2008 2574 2582
2. M. Bandell, G.M. Story, S.W. Hwang, V. Viswanath, S.R. Eid, M.J. Petrus, T.J. Earley, and A. Patapoutian Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin Neuron 41 2004 849 857
3. A. Banvolgyi, G. Pozsgai, S.D. Brain, Z.S. Helyes, J. Szolcsanyi, M. Ghosh, B. Melegh, and E. Pinter Mustard oil induces a transient receptor potential vanilloid 1 receptor-independent neurogenic inflammation and a non-neurogenic cellular inflammatory component in mice Neuroscience 125 2004 449 459
4. P.G. Baraldi, D. Preti, S. Materazzi, and P. Geppetti Transient receptor potential ankyrin 1 (TRPA1) channel as emerging target for novel analgesics and anti-inflammatory agents J Med Chem 53 2010 5085 5107
5. T. Bartsch, and P.J. Goadsby Increased responses in trigeminocervical nociceptive neurons to cervical input after stimulation of the dura mater Brain 126 2003 1801 1813
6. D.M. Bautista, S.E. Jordt, T. Nikai, P.R. Tsuruda, A.J. Read, J. Poblete, E.N. Yamoah, A.I. Basbaum, and D. Julius TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents Cell 124 2006 1269 1282
7. D.M. Bautista, P. Movahed, A. Hinman, H.E. Axelsson, O. Sterner, E.D. Hogestatt, D. Julius, S.E. Jordt, and P.M. Zygmunt Pungent products from garlic activate the sensory ion channel TRPA1 Proc Natl Acad Sci USA 102 2005 12248 12252
8. S. Benemei, G. Appendino, and P. Geppetti Pleasant natural scent with unpleasant effects: cluster headache-like attacks triggered by Umbellularia californica Cephalalgia 30 2010 744 746
9. B.F. Bessac, and S.E. Jordt Breathtaking TRP channels: TRPA1 and TRPV1 in airway chemosensation and reflex control Physiology (Bethesda) 23 2008 360 370
10. R. Burstein, M. Jakubowski, E. Garcia-Nicas, V. Kainz, Z. Bajwa, R. Hargreaves, L. Becerra, and D. Borsook Thalamic sensitization transforms localized pain into widespread allodynia Ann Neurol 68 2010 81 91
11. N.M. Carmichael, M.P. Charlton, and J.O. Dostrovsky Activation of the 5-HT1B/D receptor reduces hindlimb neurogenic inflammation caused by sensory nerve stimulation and capsaicin PAIN® 134 2008 97 105
12. C.H. Chou, A.C. Chao, S.R. Lu, H.H. Hu, and S.J. Wang Cephalic venous congestion aggravates only migraine-type headaches Cephalalgia 24 2004 973 979
13. C.H. Chou, J.L. Fuh, H.H. Hu, J.C. Wu, and S.J. Wang Throbbing pain is related to Queckenstedt's test effect in migraine patients Cephalalgia 29 2009 373 378
14. D.P. Corey, J. Garcia-Anoveros, J.R. Holt, K.Y. Kwan, S.Y. Lin, M.A. Vollrath, A. Amalfitano, E.L. Cheung, B.H. Derfler, A. Duggan, G.S. Geleoc, P.A. Gray, M.P. Hoffman, H.L. Rehm, D. Tamasauskas, and D.S. Zhang TRPA1 is a candidate for the mechanosensitive transduction channel of vertebrate hair cells Nature 432 2004 723 730
15. J.P. Courteau, R. Cushman, F. Bouchard, M. Quevillon, A. Chartrand, and L. Bherer Survey of construction workers repeatedly exposed to chlorine over a three to six month period in a pulpmill: I. Exposure and symptomatology Occup Environ Med 51 1994 219 224
16. L. Cruz-Orengo, A. Dhaka, R.J. Heuermann, T.J. Young, M.C. Montana, E.J. Cavanaugh, D. Kim, and G.M. Story Cutaneous nociception evoked by 15-delta PGJ2 via activation of ion channel TRPA1 Mol Pain 4 2008 30
17. D.S. da Costa, F.C. Meotti, E.L. Andrade, P.C. Leal, E.M. Motta, and J.B. Calixto The involvement of the transient receptor potential A1 (TRPA1) in the maintenance of mechanical and cold hyperalgesia in persistent inflammation PAIN® 148 2010 431 437
18. Y. Dai, S. Wang, M. Tominaga, S. Yamamoto, T. Fukuoka, T. Higashi, K. Kobayashi, K. Obata, H. Yamanaka, and K. Noguchi Sensitization of TRPA1 by PAR2 contributes to the sensation of inflammatory pain J Clin Invest 117 2007 1979 1987
19. de Lima AM, Sapienza GB, Giraud Vde O, Fragoso YD. Odors as triggering and worsening factors for migraine in men. Arq Neuropsiquiatr 2011;69:324-7.
20. D. del Camino, S. Murphy, M. Heiry, L.B. Barrett, T.J. Earley, C.A. Cook, M.J. Petrus, M. Zhao, M. D'Amours, N. Deering, G.J. Brenner, M. Costigan, N.J. Hayward, J.A. Chong, C.M. Fanger, C.J. Woolf, A. Patapoutian, and M.M. Moran TRPA1 contributes to cold hypersensitivity J Neurosci 30 2010 15165 15174
21. R.M. Edelmayer, T.W. Vanderah, L. Majuta, E.T. Zhang, B. Fioravanti, M. De Felice, J.G. Chichorro, M.H. Ossipov, T. King, J. Lai, S.H. Kori, A.C. Nelsen, K.E. Cannon, M.M. Heinricher, and F. Porreca Medullary pain facilitating neurons mediate allodynia in headache-related pain Ann Neurol 65 2009 184 193
22. S.R. Eid, E.D. Crown, E.L. Moore, H.A. Liang, K.C. Choong, S. Dima, D.A. Henze, S.A. Kane, and M.O. Urban HC-030031, a TRPA1 selective antagonist, attenuates inflammatory- and neuropathy-induced mechanical hypersensitivity Mol Pain 4 2008 48
23. O. Fajardo, V. Meseguer, C. Belmonte, and F. Viana TRPA1 channels mediate cold temperature sensing in mammalian vagal sensory neurons: pharmacological and genetic evidence J Neurosci 28 2008 7863 7875
24. B. Fioravanti, A. Kasasbeh, R. Edelmayer, D.P. Skinner Jr, J.A. Hartings, R.D. Burklund, M. De Felice, E.D. French, G.O. Dussor, D.W. Dodick, F. Porreca, and T.W. Vanderah Evaluation of cutaneous allodynia following induction of cortical spreading depression in freely moving rats Cephalalgia 31 2011 1090 1100
25. D.I. Friedman, and T. De ver Dye Migraine and the environment Headache 49 2009 941 952
26. S.E. Jordt Trigeminal TRPs and the scent of pain PAIN® 152 2011 4 5
27. S.E. Jordt, D.M. Bautista, H.H. Chuang, D.D. McKemy, P.M. Zygmunt, E.D. Hogestatt, I.D. Meng, and D. Julius Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1 Nature 427 2004 260 265
28. L. Kelman The triggers or precipitants of the acute migraine attack Cephalalgia 27 2007 394 402
29. P.C. Kerstein, D. del Camino, M.M. Moran, and C.L. Stucky Pharmacological blockade of TRPA1 inhibits mechanical firing in nociceptors Mol Pain 5 2009 19
30. Y.S. Kim, J.Y. Son, T.H. Kim, S.K. Paik, Y. Dai, K. Noguchi, D.K. Ahn, and Y.C. Bae Expression of transient receptor potential ankyrin 1 (TRPA1) in the rat trigeminal sensory afferents and spinal dorsal horn J Comp Neurol 518 2010 687 698
31. W.M. Knowlton, A. Bifolck-Fisher, D.M. Bautista, and D.D. McKemy TRPM8, but not TRPA1, is required for neural and behavioral responses to acute noxious cold temperatures and cold-mimetics in vivo PAIN® 150 2010 340 350
32. B. Kremeyer, F. Lopera, J.J. Cox, A. Momin, F. Rugiero, S. Marsh, C.G. Woods, N.G. Jones, K.J. Paterson, F.R. Fricker, A. Villegas, N. Acosta, N.G. Pineda-Trujillo, J.D. Ramirez, J. Zea, M.W. Burley, G. Bedoya, D.L. Bennett, J.N. Wood, and A. Ruiz-Linares A gain-of-function mutation in TRPA1 causes familial episodic pain syndrome Neuron 66 2010 671 680
33. P.E. Kunkler, C.J. Ballard, G.S. Oxford, and J.H. Hurley TRPA1 receptors mediate environmental irritant-induced meningeal vasodilatation PAIN® 152 2011 38 44
34. K.Y. Kwan, J.M. Glazer, D.P. Corey, F.L. Rice, and C.L. Stucky TRPA1 modulates mechanotransduction in cutaneous sensory neurons J Neurosci 29 2009 4808 4819
35. S. Materazzi, R. Nassini, E. Andre, B. Campi, S. Amadesi, M. Trevisani, N.W. Bunnett, R. Patacchini, and P. Geppetti Cox-dependent fatty acid metabolites cause pain through activation of the irritant receptor TRPA1 Proc Natl Acad Sci USA 105 2008 12045 12050
36. D.J. Matson, D.C. Broom, and D.N. Cortright Locomotor activity in a novel environment as a test of inflammatory pain in rats Methods Mol Biol 617 2010 67 78
37. C.R. McNamara, J. Mandel-Brehm, D.M. Bautista, J. Siemens, K.L. Deranian, M. Zhao, N.J. Hayward, J.A. Chong, D. Julius, M.M. Moran, and C.M. Fanger TRPA1 mediates formalin-induced pain Proc Natl Acad Sci USA 104 2007 13525 13530
38. M. Mitrovic, A. Shahbazian, E. Bock, M.A. Pabst, and P. Holzer Chemo-nociceptive signalling from the colon is enhanced by mild colitis and blocked by inhibition of transient receptor potential ankyrin 1 channels Br J Pharmacol 160 2010 1430 1442
39. C. Nassenstein, K. Kwong, T. Taylor-Clark, M. Kollarik, D.M. Macglashan, A. Braun, and B.J. Undem Expression and function of the ion channel TRPA1 in vagal afferent nerves innervating mouse lungs J Physiol 586 2008 1595 1604
40. R. Nassini, S. Materazzi, E. Andre, L. Sartiani, G. Aldini, M. Trevisani, C. Carnini, D. Massi, P. Pedretti, M. Carini, E. Cerbai, D. Preti, G. Villetti, M. Civelli, G. Trevisan, C. Azzari, S. Stokesberry, L. Sadofsky, L. McGarvey, R. Patacchini, and P. Geppetti Acetaminophen, via its reactive metabolite N-acetyl-p-benzo-quinoneimine and transient receptor potential ankyrin-1 stimulation, causes neurogenic inflammation in the airways and other tissues in rodents FASEB J 24 2010 4904 4916
41. R. Nassini, S. Materazzi, G. De Siena, F. De Cesaris, and P. Geppetti Transient receptor potential channels as novel drug targets in respiratory diseases Curr Opin Investig Drugs 11 2010 535 542
42. R. Nassini, S. Materazzi, J. Vriens, J. Prenen, S. Benemei, G. De Siena, G. la Marca, E. Andre, D. Preti, C. Avonto, L. Sadofsky, V. Di Marzo, L. De Petrocellis, G. Dussor, F. Porreca, O. Taglialatela-Scafati, G. Appendino, B. Nilius, and P. Geppetti The "headache tree" via umbellulone and TRPA1 activates the trigeminovascular system Brain 135 2012 376 390
43. M.L. Oshinsky, and S. Gomonchareonsiri Episodic dural stimulation in awake rats: a model for recurrent headache Headache 47 2007 1026 1036
44. Peyrot des Gachons C, Uchida K, Bryant B, Shima A, Sperry JB, Dankulich-Nagrudny L, Tominaga M, Smith AB III, Beauchamp GK, Breslin PA. Unusual pungency from extra-virgin olive oil is attributable to restricted spatial expression of the receptor of oleocanthal. J Neurosci 2011;31:999-1009.
45. I.M. Ritchie, and R.G. Lehnen Formaldehyde-related health complaints of residents living in mobile and conventional homes Am J Public Health 77 1987 323 328
46. M. Schmidt, A.E. Dubin, M.J. Petrus, T.J. Earley, and A. Patapoutian Nociceptive signals induce trafficking of TRPA1 to the plasma membrane Neuron 64 2009 498 509
47. E.S. Schwartz, J.A. Christianson, X. Chen, J.H. La, B.M. Davis, K.M. Albers, and G.F. Gebhart Synergistic role of TRPV1 and TRPA1 in pancreatic pain and inflammation Gastroenterology 140 2011 e1281 e1282
48. W.F. Stewart, R.B. Lipton, A.J. Dowson, and J. Sawyer Development and testing of the Migraine Disability Assessment (MIDAS) Questionnaire to assess headache-related disability Neurology 56 2001 S20 S28
49. N.L. Stucky, E. Gregory, M.K. Winter, Y.Y. He, E.S. Hamilton, K.E. McCarson, and N.E. Berman Sex differences in behavior and expression of CGRP-related genes in a rodent model of chronic migraine Headache 51 2011 674 692
50. 2 Nat Chem Biol 7 2011 701 711
51. T.E. Taylor-Clark, S. Ghatta, W. Bettner, and B.J. Undem Nitrooleic acid, an endogenous product of nitrative stress, activates nociceptive sensory nerves via the direct activation of TRPA1 Mol Pharmacol 75 2009 820 829
52. T.E. Taylor-Clark, B.J. Undem, D.W. Macglashan Jr, S. Ghatta, M.J. Carr, and M.A. McAlexander Prostaglandin-induced activation of nociceptive neurons via direct interaction with transient receptor potential A1 (TRPA1) Mol Pharmacol 73 2008 274 281
53. M. Trevisani, J. Siemens, S. Materazzi, D.M. Bautista, R. Nassini, B. Campi, N. Imamachi, E. Andre, R. Patacchini, G.S. Cottrell, R. Gatti, A.I. Basbaum, N.W. Bunnett, D. Julius, and P. Geppetti 4-Hydroxynonenal, an endogenous aldehyde, causes pain and neurogenic inflammation through activation of the irritant receptor TRPA1 Proc Natl Acad Sci USA 104 2007 13519 13524
54. L.P. Vera-Portocarrero, M.H. Ossipov, T. King, and F. Porreca Reversal of inflammatory and noninflammatory visceral pain by central or peripheral actions of sumatriptan Gastroenterology 135 2008 1369 1378
55. V.C. Wallace, J. Blackbeard, A.R. Segerdahl, F. Hasnie, T. Pheby, S.B. McMahon, and A.S. Rice Characterization of rodent models of HIV-gp120 and anti-retroviral-associated neuropathic pain Brain 130 2007 2688 2702
56. X. Wei, R.M. Edelmayer, J. Yan, and G. Dussor Activation of TRPV4 on dural afferents produces headache-related behavior in a preclinical rat model Cephalalgia 31 2011 1595 1600
57. J. Wieseler, A. Ellis, D. Sprunger, K. Brown, A. McFadden, J. Mahoney, N. Rezvani, S.F. Maier, and L.R. Watkins A novel method for modeling facial allodynia associated with migraine in awake and freely moving rats J Neurosci Methods 185 2010 236 245
58. J. Yan, R.M. Edelmayer, X. Wei, M. De Felice, F. Porreca, and G. Dussor Dural afferents express acid-sensing ion channels: a role for decreased meningeal pH in migraine headache PAIN® 152 2011 106 113
59. J. Zhong, A. Minassi, J. Prenen, O. Taglialatela-Scafati, G. Appendino, and B. Nilius Umbellulone modulates TRP channels Pflugers Arch 462 2011 861 870
60. G. Ziem, and J. McTamney Profile of patients with chemical injury and sensitivity Environ Health Perspect 105 1997 417 436